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Welcome to the CLU-IN Internet Seminar

Arsenic - Health and Remediation Applications, Session 2 - Emerging Issues in Arsenic Exposure and Disease

Sponsored by: NIEHS Superfund Research ProgramDelivered: November 2, 2012, 2:00 PM - 4:00 PM, EDT (19:00-21:00

GMT)

Instructors:Allan H. Smith, M.D., Ph.D., University of California, Berkeley, School of Public Health

(ahsmith@berkeley.edu)Joshua W. Hamilton, Ph.D., Dartmouth College SRP Center (jhamilton@mbl.edu)

Moderator:

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The Astonishing Long-Term Effects of The Astonishing Long-Term Effects of In UteroIn Utero & & Early Childhood Exposure to ArsenicEarly Childhood Exposure to Arsenic

Allan H. Smith MD, PhDProfessor of Epidemiology

University of California, Berkeley

Recent findings from the Arsenic Health Effects Research Program

With support from NIH including the NIEHS Superfund Program

The Berkeley Arsenic Health Effects The Berkeley Arsenic Health Effects Research Group (ASRGResearch Group (ASRG))

Arsenic Research Group

Not

Allan Smith’s Research Group

Associate Director: Craig SteinmausAssociate Director: Craig Steinmaus

When I first started research on arsenic in water When I first started research on arsenic in water over 20 years ago, we only knew it caused skin over 20 years ago, we only knew it caused skin

lesions and skin cancer.lesions and skin cancer.

Lung cancer and arsenic in TaiwanLung cancer and arsenic in Taiwanadapted from CJ Chen et al 1988

0

1

2

3

4

5

6

7

8

9

women men

all Taiwan170 ug/L470 ug/L800 ug/L

• Comparison population, all of Taiwan

• vertical axis: age adjusted rate ratios (relative risk)

It is surprising that arsenic in It is surprising that arsenic in drinking water would have major drinking water would have major

effects in the lungseffects in the lungs

Known causes of lung cancer involve Known causes of lung cancer involve inhalationinhalation

• smoking• passive smoking• asbestos• radon• silica• chromium

• diesel exhaust• coke oven PAHs• bischlormethyl ether• nickel• arsenic

Cancer risks from arsenic in drinking Cancer risks from arsenic in drinking waterwater

At the current standard of 50 ug/L, the lifetime risk of dying from cancer from drinking 1 L/day of water could be as

high as 13 per 1000 persons

Environmental Health Perspectives 97:259-267, 1992

Martyn Smith

The lost and forgottenThe lost and forgottenarsenic-exposed populationarsenic-exposed population

“the number of people consuming water from private wells with arsenic concentrations above 10 µg/L

could be over 2 million people”

Where is this population?

Right here in the USA

Steinmaus et al. In Press.

0

100

200

300

400

500

- 100 200 300 400 500

Hach

Quick

Laboratory Arsenic (g/L)

Fie

ld T

est

Kit

Arse

nic

(

g/L

)

0

There are high concentrations of arsenic in private wells in There are high concentrations of arsenic in private wells in the U.S. toothe U.S. too

Steinmaus CM, George CM, Kalman DA, Smith AH. Environ Sci Technology, 40:3362-3366, 2006

People with private wells are on their ownPeople with private wells are on their own

0

100

200

300

400

500

600

700

800

900

1000

Pre-filter Post-filter

Arsen

ic c

on

cen

trati

on

(u

g/L

)

Gearoge CM …… Steinmaus C. Arch Environ Occup Health 61:171-175, 2006.

CHILE

Region II

Region V

Age Group 30-39 40-49 50-59 60-69 70-79 SMR p value

WomenObserved 5 23 21 41 47Expected 1.2 3.0 8.0 16.0 13.3O/E 4.2 7.7 2.6 2.6 3.5 3.1 p<0.001

MenObserved 14 48 142 177 129Expected 1.2 8.1 28.5 61.8 32.1O/E 11.7 5.9 4.9 2.9 4.0 3.8 p<0.001

Lung Cancer Mortality Region II Chile, 1989-1993

Smith et al. American Journal of Epidemiology, 1998.Smith AH et al. American Journal of Epidemiology, 1998. Mario Goycolea

Lung Cancer and Inhalation of Arsenic

0

1

2

3

4

5

6

7

8

9

0 200 400 600 800 1000 1200

Urinary arsenic (ug/l)

Enterline PE et al, Am J Epidemiol 1987;125:929-38

Lu

ng

can

cer

SM

R

Lung cancer relative risk estimates from a case-contol study in Chile

(Ferreccio et al, Epidemiology, 2000)

0

1

2

3

4

5

6

7

8

9

0 100 200 300 400 500 600 700 800 900

Water Arsenic Concentration

Rela

tive R

isk

0.0

2.0

4.0

6.0

8.0

10.0

12.0

0 200 400 600 800 1,000 1,200 1,400

Urinary Arsenic Concentration (g/Liter)

Rela

tive R

isk o

f Lung C

ancer

Ingested Arsenic

Inhaled Arsenic

Linear (Ingested Arsenic)

Linear (Inhaled Arsenic)

Smith AH, Ercumen A, Yuan Y, Steinmaus CM.. J Exposure Science and Environmental Epidemiology 19:343-8, 2009

Increased lung cancer risks are similar whether Increased lung cancer risks are similar whether arsenic is ingested or inhaled.arsenic is ingested or inhaled.

The estimated cancer risk at the drinking water The estimated cancer risk at the drinking water standard of 50 µg/L for arsenic is more than 100 standard of 50 µg/L for arsenic is more than 100 times greater than that for any other drinking times greater than that for any other drinking

water contaminantwater contaminant

Smith AH, Lopipero PA, Bates MN, Steinmaus CM.

Arsenic epidemiology and drinking water standards.

Science 296: 2145-6, 2002

Cancer risk from contaminants in drinking water other than arsenic

0

2

4

6

8

10

12

14

Per 100,000

Top of the list:

Ethylene dibromide

Cancer risk from contaminants in drinking water including arsenic

0

200

400

600

800

1000

1200

1400

Per 100,000

Cancer risks fromarsenic at the olddrinking water standardwere >100 times higherthan the next highestrisk contaminant

Cancer risks from arsenic in drinking waterCancer risks from arsenic in drinking water

• 10 ug/L 1 in 500 die• 50 ug/L 1 in 100 die• 500 ug/L 1 in 10

die• 5000 ug/L all die

Lung cancer and smoking

married to a smoker

active smoker

And arsenic in water looks good, does not smelland has no taste. So the risks are unbelievable

Marshall G, Ferreccio C, et al.

Fifty-year study of lung and bladder cancer mortality in Chile related to arsenic in drinking water. J Natl Cancer Inst 99:920-928, 2007

Mortality data were already available computerized for 1971-2000.

For the years 1950-1971, 200,000 death certificates were digitally photographed and coded for this study.

Mortality from lung cancer among men, Mortality from lung cancer among men, Region II Chile Region II Chile Marshall et al, J. Natl Cancer Inst, 2007Marshall et al, J. Natl Cancer Inst, 2007

0

1

2

3

4

5

1950 1960 1970 1980 1990 2000

Year

Ra

te R

ati

os

Rate ratios Lower 95% CI Upper 95% CI

Peak exposure

started stopped

So what do we now think arsenic in drinking So what do we now think arsenic in drinking water causes?water causes?

• Respiratory Cancers of the lung and larynx, reduced lung function, bronchiectasis, chronic

cough and shortness of breath. Tuberculosis mortality increased?

• Renal tract Bladder and kidney cancer, chronic renal failure

• Cardiovascular Myocardial infarction, cerebrovascular effects, hypertension.

• Neurological Peripheral neuropathy, reduced cognitive function in children

• Other Skin pigmentation changes, skin cancer, liver cancer, diabetes

Effect of early life exposureEffect of early life exposure

In utero

and in the first few years of childhood

Source: Project Well, West Bengal, India, 2003

Arsenic concentrations in drinking water in Arsenic concentrations in drinking water in the city of Antofagasta (popn 200,000) in the city of Antofagasta (popn 200,000) in

ChileChile

All childhood cancers

0

5

10

15

Year of Birth

RR

Boys

Girls

Boys 1 0.7 0.9

Girls 1 1 1.2

1950-1957 1958-1970 1971-1981

Liver cancer

0

5

10

15

Year of Birth

RR

Boys

Girls

Boys 8.9 1.2 1.1

Girls 14.1 1.2 3.2

1950-1957 1958-1970 1971-1981

p=0.01

Liaw J, et al Increased childhood liver cancer mortality and arsenic in drinking water in northern Chile. Cancer Epidemiol Biomarkers Prev. 2008.

Lung cancer mortality in men accordingto exposure in childhood

| | | | | |1950 1960 1970 1980 1990 2000

peak arsenic

|born

| |1989 1998

Lung cancer mortality in older men (SMR = standardized mortality ratio = observed/expected deaths)

0

2

4

6

8

10

12

14

rest Chile exposed | | | | | |1950 1960 1970 1980 1990 2000

peak arsenic

|born1920-38

| |1989 1998

Age at death 60 – 69

p < 0.001

SMR

Lung cancer mortality in men accordingto exposure in childhood

(SMR = standardized mortality ratio = observed/expected deaths)

0

2

4

6

8

10

12

14

rest Chile exposed | | | | | |1950 1960 1970 1980 1990 2000

peak arsenic

| born1953-57

| |1989 1998

Age at death 35 – 39

p < 0.001

SMR

Lung cancer mortality in men accordingto exposure in childhood

(SMR = standardized mortality ratio = observed/expected deaths)

0

2

4

6

8

10

12

14

rest Chile exposed | | | | | |1950 1960 1970 1980 1990 2000

peak arsenic

|bornafter 1957

| |1989 1998

Age at death 30 – 34

p < 0.001

SMR

012

34

56

78

9

atombomb

ETS arsenic

• Atomic bomb survivors Hiroshima and Nagasaki aged 10-20 in 1945. No cases in those exposed in utero or under age 10.

• A study giving lung cancer relative risks in the age range 30-39 following many hours of daily passive smoking as children (only four cases).

• Lung cancer relative risks in age range 30-39 in Region II of Chile following early life exposure to arsenic in water. There were 32 lung cancer deaths with 3.8 expected (RR=8.4, p<0.001).

Childhood exposures and young adult lung cancer relative Childhood exposures and young adult lung cancer relative risksrisks

Smith AH et al. Environmental Health Perspectives 2006

End Stage Lung DiseaseEnd Stage Lung Disease

Obstruction, Infection, Hemoptysis, Bronchiectasis

High resolution computed tomography (HRCT) with readings in India and the United States without knowing who had arsenic skin lesions.

Dr. D. N. Guha Mazumder

Craig Steinmaus

Study design, x-ray (HRCT) study in West Bengal, IndiaStudy design, x-ray (HRCT) study in West Bengal, India

Referred forHRCT

Assessed inthis study

10-fold increased prevalence of bronchiectasis OR=10.1, p<0.01Epidemiology 2005

Lung function findings of Lung function findings of reduced FEV1 adjusted for age reduced FEV1 adjusted for age

and heightand height

-300

-250

-200

-150

-100

-50

0

men skinlesions

men,smoking

women,skin

lesions

• For all men combined P=0.007

• Among men in this population, arsenic- caused skin lesions were associated with a greater FEV1 reduction (-256ml) than from smoking (-156ml)

Von Ehrenstein OS et al. Am J Epidemiol 162: 533-41, 2005

Mortality (SMRs) from Chronic Obstructive Pulmonary Disease, age 30-49, for those born in the very high

exposure period (in utero exposure) or just before (child)

0

5

10

15

20

25

30

35

40

45

50

All COPD

All

in utero

child

05

101520253035404550

Bronchiectasis

Allin uterochild

0

510

15

20

2530

35

40

4550

Other COPD

Allin uterochild

p<0.001 except other COPD p=0.004

A dugwell with modified design to reduceA dugwell with modified design to reducebacterial contaminationbacterial contamination

Intervention program in West BengalIntervention program in West BengalDirector: Meera HiraSmithDirector: Meera HiraSmith

• Modern design dugwell program to provide arsenic free water in West Bengal

• Funded by private donors

• for more information http://www.projectwellusa.org

Distribution of Children’s Arsenic Exposure (ug/L) In Utero

Excess deaths among men in Region II of Chile Excess deaths among men in Region II of Chile from acute MI, lung cancer and bladder cancer.from acute MI, lung cancer and bladder cancer.

Yuan Y et al. Am J Epidemiol 166:1381-1391, 2007

0

2

4

6

8

10

12

1950-1957 1958-1964 1965-1970 1971-1979 1980-1985 1986-1990 1991-1995 1996-2000

Years

Excess d

eath

s (

%)

Acute Myocardial Infarction Lung Cancer Bladder Cancer

Male

At the peak more than 1 in 10 of all deaths were due to arsenic

Early life exposure and myocardial infarction Early life exposure and myocardial infarction mortality in young adultsmortality in young adults

The highest rate ratios were for young adult men aged 30–49 years who were born during the high-exposure period with probable exposure in utero and in early childhood (rate ratio = 3.23, 95% CI: 2.79, 3.75; p < 0.001)

Yuan Y et al. Am J Epidemiol 2007

CANCER MORTALITY

NON-CANCER MORTALITY

SMR=2.7, p<0.001

Bladder Cancer

Larynx Cancer

Lung Cancer

Kidney Cancer

Liver Cancer

Bronchiectasis

Other COPD

Acute myocardial infarction

Chronic renal disease

SMR=21.3, p<0.001

SMR=10.5, p<0.001

SMR=6.8, p<0.001

SMR=3.4, p<0.001

SMR=3.1, p<0.001

SMR=25.1, p<0.001

SMR=4.5, p<0.001

SMR=2.4, p<0.001

Rest of Chile

Increased non-cancer mortality due to arsenic

0 5 10 15 20 25 30

Standardized mortality ratios (SMRs)

Increased cancer mortality due to arsenic

Ecologic study of mortality of young adults aged 30-49 Ecologic study of mortality of young adults aged 30-49 following exposure to high concentrations of arsenic in following exposure to high concentrations of arsenic in

drinking water in early lifedrinking water in early life(not yet published)(not yet published)

Scientific plausibility

Studies in mice by NIEHS have shown increased tumors in offspring of mice dosed with 85,000 ug/L, including bladder and lung tumors.(e.g. Tokar EJ, Diwan BA, Waalkes MP. Toxicology Letters 209:179– 185, 2012)

The very high doses were given to achieve internal organ concentrations similar to highly exposed humans.

Extrapolating risk to lower exposureExtrapolating risk to lower exposure

• The exposures involved in Chile were to 850ug/L.

• Some risks might be detectable by very large epidemiology studies with exposure around 100 ug/L

• Even if there are risks at less than 50 ug/L, it is unlikely that epidemiological studies would ever find them

• We need to think in terms of extrapolation of risks downwards and margins of safety

Early life exposure to high concentrations of arsenic in water has major impact on young adult

mortality beyond that from any other environmental exposure

The END

Note: Funding for these studies was provided by NIEHS research grants including the Superfund Research

Program

JWH 04/19/23

MOUSE MODELS OF HUMAN IN UTERO AND ADULT EXPOSURES TO LOW-DOSE

ARSENIC

Joshua W. Hamilton Ph.D.Senior Scientist, Bay Paul Center,

Marine Biological Laboratory (MBL), Woods Hole MA

Professor, Pathology & Laboratory Medicine, Brown University, Providence RI

Project Leader, Dartmouth’s Superfund Research Program

on Toxic Metals, Hanover NH

JWH 04/19/23

Arsenic and Old Concerns

“It is an uncanny thought that this lurking poison (arsenic) is everywhere around us, ready to gain unsuspected entrance to our

bodies in the food we eat, the water we drink and the air we breathe.”

Karl Vogel, 1928

JWH 04/19/23

METALS: Toxic Metals, Heavy Metals, Essential Metals

•three-fourths of all elements are metals or metalloids

•a “heavy metal” refers to its atomic weight, not its toxicity

•many metals are essential or play a normal role in biology

•many toxic metals that are not essential can mimic essential metals

•like all chemicals, all metals are toxic at high enough doses

•like all chemicals, all metals are non-toxic at very low doses

JWH 04/19/23

Toxic metals in the environment

• Toxic metals are a major concern at both Superfund / toxic waste sites and in the environment in general

• Eight of the top fifty substances on the CDC’s ATSDR priority list are metals, including the top three chemicals of concern in the environment: arsenic, lead and mercury

• Eight of the twenty-two substances on the EPA’s OSWER list of chemicals of highest concern at Superfund sites are metals: arsenic, lead, mercury, cadmium, chromium, nickel, zinc and copper

JWH 04/19/23

Arsenic: “poison of kings and king of poisons”

• Ancient Rome - Women’s club used arsenic to poison husbands

• Renaissance - The Borgias used arsenic to poison rivals and increase their wealth

• Were Napolean and Mozart poisoned by arsenic?

Cesare Borgia

“The death of Napolean”a lock of Napolean’s hair

JWH 04/19/23

Arsenic as an environmental contaminant

• Previous US and WHO drinking water standard (Maximum Contaminant Level, MCL) for arsenic was 50 parts per billion (ppb) from 1950’s through 2001

• US recently lowered MCL to 10 ppb (Jan. 2006), but 7-14 year implementation

• current WHO and EU arsenic standard is 10 ppb

• WHO program of digging tube wells in India, Bangledesh to alleviate cholera problem led to massive population exposure to excess arsenic in drinking water

• highly contaminated areas (India, South America) can contain as much as 1800 ppb (180 times the WHO standard)

• Estimated 250 million to 1 billion people affected worldwide by excess arsenic

JWH 04/19/23

Arsenic as a causative agent in human disease

• Chronic human exposure to inorganic arsenic at sub-acute doses has been linked to increased risk of:

• Cancers- esp. lung, skin and bladder but also liver, kidney, and other malignancies

• Diabetes (type 2, non-insulin-dependent, “adult-onset”)

• Vascular and cardiovascular disease• Reproductive and developmental problems• Neurological problems

• U.S. & South America - range is typically 1-100 ppb

• Asia - range is typically 10-1000 ppb

JWH 04/19/23

Arsenic as an environmental contaminant in New England

• In New Hampshire, ~40% of the population gets its drinking water from private, unregulated wells

• Of these wells, greater than one in five has excess arsenic, representing about 10% of the state’s population (~120,000 people)

• Similar ratios are found in Maine (~150,000 people)

• In the U.S. as a whole, as many as 25 million people may be drinking excess arsenic in their drinking water

• NH and ME also have elevated levels of arsenic in soil both naturally and from lead arsenate pesticide use (avg. 20 ppm vs. 1-5 ppm in most of U.S.)

JWH 04/19/23

Center for Environmental

Health Sciences at Dartmouth

Dartmouth

TOXIC METALSResearch Program

Project 8 - Bruce StantonProject 8 - Bruce Stantonmolecular toxicology of molecular toxicology of

arsenicarsenic

Project 2 - Joshua Project 2 - Joshua HamiltonHamilton

molecular toxicology of molecular toxicology of arsenicarsenic

Project 4 - Margaret Project 4 - Margaret KaragasKaragas

epidemiology of arsenicepidemiology of arsenicProject 7 - Carol Folt & Celia Project 7 - Carol Folt & Celia

ChenChenecotoxicology of metalsecotoxicology of metals

“Toxic Metals in the Northeast”

NIH-NIEHS Sponsored Dartmouth

Superfund Basic Research Program

Project on Toxic Metals

An interdisciplinary research program on toxic metals in the environment and their impact on ecosystems and human health

Project 9 – Tracy Punshon & Project 9 – Tracy Punshon & MaryLou GuerinotMaryLou Guerinot

uptake of arsenic by riceuptake of arsenic by rice

JWH 04/19/23

Arsenic as an endocrine disruptor

What is an endocrine disruptor?

“Collectively, chemicals with the potential to interfere with the function of endocrine systems are called endocrine disrupting chemicals (EDCs). EDCs have been defined as exogenous agents that interfere with the production, release, transport, metabolism, binding, action, or elimination of the natural hormones in the body responsible for the maintenance of homeostasis and the regulation of developmental processes.”

Strategic Research Plan for Endocrine Disruptors, 1998

Office of Research and DevelopmentU.S. EPA

JWH 04/19/23

Hormone receptor biology and endocrine disruption

organic Endocrine Disrupting Chemicals- EDCs (pesticides, etc.)

competitive agonists - mimic hormone, bind to receptor, activate receptor

competitive antagonists - mimic hormone, bind to receptor, block normal hormone binding and activation

JWH 04/19/23

Arsenic has opposite effects on steroid receptor function

at lower (0.01-1.0 µM) and higher (2-3 µM) doses

JE Bodwell et al. Chem Res Toxicol 17:1064-1076, 2004

No Observed Effect Level(NOEL)

No Observed Effect Level(NOEL)

50-90% suppression -2-3 µM,140-210 ppb

2-2.5 fold enhancement -0.01-1 µM,0.7-70 ppb

JWH 04/19/23

Human Age (month) -6 -4 -2 0 2 4 6 8 10 12 14

Pla

sm

a T

H

25

50

75

100

Xenopus Stage

35/36 45 51 55 58 61 63 66

Metamorphic ClimaxPrometamorphosisPremetamorphosis

Human

Xenopus

TR active

As

YB Shi. et al.(2002) Pharmacol Ther 94:235-251

Thyroid hormone mediated metamorphosis - Xenopus

JWH 04/19/23

Effects of arsenic on thyroid hormone-mediated ex vivo tail shrinkage in Xenopus

JC Davey et al. Environ Hlth Perspect 116:165-172, 2008

JWH 04/19/23

Summary of arsenic as an endocrine disruptor

• Arsenic affects all five steroid hormone receptors:• Estrogen Receptor• Progesterone Receptor• Androgen (Testosterone) Receptor• Glucocorticoid (Cortisol) Receptor• Mineralocorticoid (Aldosterone) Receptor

• Arsenic affects other nuclear hormone receptors:• Retinoic Acid Receptor• Thyroid Hormone Receptor• PPAR Receptors

• Arsenic enhances hormone signaling at very low doses

• Arsenic suppresses hormone signaling at higher doses

JWH 04/19/23

Arsenic and lung disease

• Arsenic exposure is associated with increased risk of:

• Lung Cancer• Bronchiectasis• COPD• Emphysema• Chronic Lung Infections

• Arsenic is unique in increasing lung disease risk via ingestion rather than (or in addition to) inhalation

• Arsenic synergistically increases risk of lung disease from other lung toxicants including tobacco smoke, environmental air contaminants, bacterial and viral infections

JWH 04/19/23

Arsenic and long-term risk of bronchiectasis in Region II of Chile

Marshall, J Natl Canc Inst 2000 -- Ferreccio, Epidemiology 2000 -- Smith, Environ Hlth Perspect 2006

JWH 04/19/23

Arsenic in drinking water (100 ppb) increases

H1N1 flu-induced morbidity in mice

CD Kozul et al., Environ Hlth Perspect 117: 1441-1447, 2009

JWH 04/19/23

Arsenic and metabolic diseases

• Arsenic exposure has been associated with:• Changes in serum cholesterol and triglycerides• Development of type 2 diabetes and other

metabolic disorders• Lower than normal birth weights• Decreases in body weight and growth during

early childhood• Vascular and cardiovascular disease

JWH 04/19/23

Effects of arsenic on mouse fetal and maternal health

CD Kozul Horvath et al., PLoS One 2012

JWH 04/19/23

Arsenic at 10 ppb in drinking water affects mouse fetal growth and development

Pregnant C57BL/6J mice were given 10 ppb arsenic in drinking water during the in utero only, post-natal weaning only, or in utero and post-natal periods

CD Kozul Horvath et al., PLoS One 2012

JWH 04/19/23

Arsenic at 10 ppb in drinking water affects mouse maternal breast milk nutrients

Pregnant C57BL/6J mice were given 10 ppb arsenic in drinking water during the in utero only, post-natal weaning only, or in utero and post-natal periods

CD Kozul Horvath et al., PLoS One 2012

JWH 04/19/23

Arsenic at 10 ppb in drinking water causes fatty liver in pregnant mice

Pregnant C57BL/6J mice were given 10 ppb arsenic in drinking water during the in utero only, post-natal weaning only, or in utero and post-natal periods

CD Kozul Horvath et al., PLoS One 2012

JWH 04/19/23

Acknowledgements

• Hamilton lab (past & present):• Ron Kaltreider• Mike Ihnat• Jennifer Davey• Tom Hampton• Athena Nomikos• Julie Gosse• Courtney Kozul-Horvath• FJ Zandbergen• Vansa Chatikavanij• Maggie Vantangoli• Adeola Adebayo

• Collaborators:• Dean Wilcox

(Dartmouth)• Jack Bodwell

(Dartmouth)• Lynn Sheldon

(Dartmouth)• Bruce Stanton

(Dartmouth)• Mike Ihnat (Oklahoma)• Richard Enelow

(Dartmouth)• Monique Depaepe

(Brown)

79

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